Oscillations and neuronal dynamics in schizophrenia: The search for basic symptoms and translational opportunities

Biological Psychiatry

Volumn 77, Issue 12, 2015, Pages 1001-1009

  Uhlhaas, Peter J ^a   Singer, Wolf ^b,c,d  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

^c ERNST STRÜNGMANN INSTITUTE ESI FOR NEUROSCIENCE IN COOPERATION WITH MAX PLANCK SOCIETY   (Germany)

^d FRANKFURT INSTITUTE FOR ADVANCED STUDIES   (Germany)

Author keywords

Cognition; Development; Dynamics; Neural oscillations; Schizophrenia; Translational research

Indexed keywords

4 AMINOBUTYRIC ACID; DOPAMINE; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

BRAIN DEVELOPMENT; BRAIN FUNCTION; BRAIN MATURATION; BRAIN NERVE CELL; BRAIN REGION; COGNITION; COGNITIVE DEFECT; COPING BEHAVIOR; DELUSION; ELECTROENCEPHALOGRAPHY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GABAERGIC TRANSMISSION; GENETIC PREDISPOSITION; GLUTAMATERGIC TRANSMISSION; HALLUCINATION; HIGH FREQUENCY OSCILLATION; HIGH RISK PATIENT; HUMAN; INTERNEURON; MAGNETOENCEPHALOGRAPHY; NEUROTRANSMISSION; NONHUMAN; POSITIVE SYNDROME; PRIORITY JOURNAL; PSYCHOSIS; REVIEW; SCHIZOPHRENIA; TRANSCRANIAL MAGNETIC STIMULATION; TRANSLATIONAL RESEARCH; ANIMAL; BRAIN; ELECTROENCEPHALOGRAM; NERVE CELL INHIBITION; NERVE CELL NETWORK; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; BRAIN; BRAIN WAVES; ELECTROENCEPHALOGRAPHY; HUMANS; NERVE NET; NEURAL INHIBITION; SCHIZOPHRENIA; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84929697243     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2014.11.019     Document Type: Review

References (113)

1. T.R. Insel Rethinking schizophrenia Nature 468 2010 187 193
2. J.A. Lieberman, T.S. Stroup, J.P. McEvoy, M.S. Swartz, R.A. Rosenheck, and D.O. Perkins Effectiveness of antipsychotic drugs in patients with chronic schizophrenia N Engl J Med 353 2005 1209 1223
3. C.A. Tamminga, R.W. Buchanan, and J.M. Gold The role of negative symptoms and cognitive dysfunction in schizophrenia outcome Int Clin Psychopharmacol 13 suppl 3 1998 S21 S26
4. M.F. Green What are the functional consequences of neurocognitive deficits in schizophrenia? Am J Psychiatry 153 1996 321 330
5. Dynamic Coordination in the Brain. Strüngmann Forum Report C. Von der Malsburg, W.A. Phillips, and W. Singer 2010 MIT Press Cambridge, MA
6. D.R. Weinberger, K.F. Berman, and R.F. Zec Physiologic dysfunction of dorsolateral prefrontal cortex in schizophrenia. I. Regional cerebral blood flow evidence Arch Gen Psychiatry 43 1986 114 124
7. A. Reichenberg The assessment of neuropsychological functioning in schizophrenia Dialogues Clin Neurosci 12 2010 383 392
8. A. Fornito, A. Zalesky, C. Pantelis, and E.T. Bullmore Schizophrenia, neuroimaging and connectomics Neuroimage 62 2012 2296 2314
9. P.J. Uhlhaas, and W. Singer Neuronal dynamics and neuropsychiatric disorders: Toward a translational paradigm for dysfunctional large-scale networks Neuron 75 2012 963 980
10. P.J. Uhlhaas, and W. Singer Abnormal neural oscillations and synchrony in schizophrenia Nat Rev Neurosci 11 2010 100 113
11. K.M. Spencer The functional consequences of cortical circuit abnormalities on gamma oscillations in schizophrenia: Insights from computational modeling Front Hum Neurosci 3 2009 33
12. G. Gonzalez-Burgos, and D.A. Lewis NMDA receptor hypofunction, parvalbumin-positive neurons and cortical gamma oscillations in schizophrenia Schizophr Bull 38 2012 950 957
13. E. Tognoli, and J.A. Kelso The metastable brain Neuron 81 2014 35 48
14. F. Varela, J.P. Lachaux, E. Rodriguez, and J. Martinerie The brainweb: Phase synchronization and large-scale integration Nat Rev Neurosci 2 2001 229 239
15. E. Bullmore, and O. Sporns Complex brain networks: Graph theoretical analysis of structural and functional systems Nat Rev Neurosci 10 2009 186 198
16. P. Fries A mechanism for cognitive dynamics: Neuronal communication through neuronal coherence Trends Cogn Sci 9 2005 474 480
17. J.F. Hipp, A.K. Engel, and M. Siegel Oscillatory synchronization in large-scale cortical networks predicts perception Neuron 69 2011 387 396
18. P.R. Roelfsema, A.K. Engel, P. König, and W. Singer Visuomotor integration is associated with zero time-lag synchronization among cortical areas Nature 385 1997 157 161
19. T.J. Buschman, E.L. Denovellis, C. Diogo, D. Bullock, and E.K. Miller Synchronous oscillatory neural ensembles for rules in the prefrontal cortex Neuron 76 2012 838 846
20. G.G. Gregoriou, S.J. Gotts, H. Zhou, and R. Desimone High-frequency, long-range coupling between prefrontal and visual cortex during attention Science 324 2009 1207 1210
21. R.F. Salazar, N.M. Dotson, S.L. Bressler, and C.M. Gray Content-specific fronto-parietal synchronization during visual working memory Science 338 2012 1097 1100
22. C.A. Bosman, J.M. Schoffelen, N. Brunet, R. Oostenveld, A.M. Bastos, and T. Womelsdorf Attentional stimulus selection through selective synchronization between monkey visual areas Neuron 75 2012 875 888
23. T. Womelsdorf, J.M. Schoffelen, R. Oostenveld, W. Singer, R. Desimone, A.K. Engel, and P. Fries Modulation of neuronal interactions through neuronal synchronization Science 316 2007 1609 1612
24. W.M. Usrey, and R.C. Reid Synchronous activity in the visual system Annu Rev Physiol 61 1999 435 456
25. H. Markram, J. Lübke, M. Frotscher, and B. Sakmann Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs Science 275 1997 213 215
26. G.Q. Bi, and M.M. Poo Synaptic modifications in cultured hippocampal neurons: Dependence on spike timing, synaptic strength, and postsynaptic cell type J Neurosci 18 1998 10464 10472
27. W. Singer Development and plasticity of cortical processing architectures Science 270 1995 758 764
28. M. Siegel, T.H. Donner, and A.K. Engel Spectral fingerprints of large-scale neuronal interactions Nat Rev Neurosci 13 2012 121 134
29. A. von Stein, and J. Sarnthein Different frequencies for different scales of cortical integration: From local gamma to long range alpha/theta synchronization Int J Psychophysiol 38 2000 301 313
30. A.K. Engel, P. König, A.K. Kreiter, and W. Singer Interhemispheric synchronization of oscillatory neuronal responses in cat visual cortex Science 252 1991 1177 1179
31. R. Vicente, L.L. Gollo, C.R. Mirasso, I. Fischer, and G. Pipa Dynamical relaying can yield zero time lag neuronal synchrony despite long conduction delays Proc Natl Acad Sci U S A 105 2008 17157 17162
32. A.K. Roopun, M.O. Cunningham, C. Racca, K. Alter, R.D. Traub, and M.A. Whittington Region-specific changes in gamma and beta2 rhythms in NMDA receptor dysfunction models of schizophrenia Schizophr Bull 34 2008 962 973
33. G. Buzsaki, and X.J. Wang Mechanisms of gamma oscillations Annu Rev Neurosci 35 2012 203 225
34. X.J. Wang Neurophysiological and computational principles of cortical rhythms in cognition Physiol Rev 90 2010 1195 1268
35. M.A. Whittington, A.K. Roopun, R.D. Traub, and C.H. Davies Circuits and brain rhythms in schizophrenia: A wealth of convergent targets Curr Opin Pharmacol 11 2011 508 514
36. B. Haider, and D.A. McCormick Rapid neocortical dynamics: Cellular and network mechanisms Neuron 62 2009 171 189
37. S. Melzer, M. Michael, A. Caputi, M. Eliava, E.C. Fuchs, M.A. Whittington, and H. Monyer Long-range-projecting GABAergic neurons modulate inhibition in hippocampus and entorhinal cortex Science 335 2012 1506 1510
38. S.R. Cobb, E.H. Buhl, K. Halasy, O. Paulsen, and P. Somogyi Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons Nature 378 1995 75 78
39. X.J. Wang, and G. Buzsaki Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model J Neurosci 16 1996 6402 6413
40. V.S. Sohal, F. Zhang, O. Yizhar, and K. Deisseroth Parvalbumin neurons and gamma rhythms enhance cortical circuit performance Nature 459 2009 698 702
41. M.A. Whittington, R.D. Traub, and J.G. Jefferys Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation Nature 373 1995 612 615
42. A.T. Lee, D. Vogt, J.L. Rubenstein, and V.S. Sohal A class of GABAergic neurons in the prefrontal cortex sends long-range projections to the nucleus accumbens and elicits acute avoidance behavior J Neurosci 34 2014 11519 11525
43. R. Rodriguez, U. Kallenbach, W. Singer, and M.H. Munk Stabilization of visual responses through cholinergic activation Neuroscience 165 2010 944 954
44. K. Dzirasa, A.J. Ramsey, D.Y. Takahashi, J. Stapleton, J.M. Potes, and J.K. Williams Hyperdopaminergia and NMDA receptor hypofunction disrupt neural phase signaling J Neurosci 29 2009 8215 8224
45. M. Krause, and Y. Jia Serotonergic modulation of carbachol-induced rhythmic activity in hippocampal slices Neuropharmacology 48 2005 381 390
46. R. Andersson, A. Johnston, and A. Fisahn Dopamine D4 receptor activation increases hippocampal gamma oscillations by enhancing synchronization of fast-spiking interneurons PLoS One 7 2012 e40906
47. A.M. Wojtowicz, L. van den Boom, A. Chakrabarty, N. Maggio, R.U. Haq, C.J. Behrens, and U. Heinemann Monoamines block kainate- and carbachol-induced gamma-oscillations but augment stimulus-induced gamma-oscillations in rat hippocampus in vitro Hippocampus 19 2009 273 288
48. J.T. Kantrowitz, and D.C. Javitt N-methyl-d-aspartate (NMDA) receptor dysfunction or dysregulation: The final common pathway on the road to schizophrenia? Brain Res Bull 83 2010 108 121
49. D.A. Lewis, T. Hashimoto, and D.W. Volk Cortical inhibitory neurons and schizophrenia Nat Rev Neurosci 6 2005 312-224
50. F.M. Benes Altered glutamatergic and GABAergic mechanisms in the cingulate cortex of the schizophrenic brain Arch Gen Psychiatry 52 1995 1015 1018 discussion 1019-1024
51. N.G. Cascella, D.J. Schretlen, and A. Sawa Schizophrenia and epilepsy: Is there a shared susceptibility? Neurosci Res 63 2009 227 235
52. J.S. Kwon, B.F. O'Donnell, G.V. Wallenstein, R.W. Greene, Y. Hirayasu, and P.G. Nestor Gamma frequency-range abnormalities to auditory stimulation in schizophrenia Arch Gen Psychiatry 56 1999 1001 1005
53. K.M. Spencer, P.G. Nestor, M.A. Niznikiewicz, D.F. Salisbury, M.E. Shenton, and R.W. McCarley Abnormal neural synchrony in schizophrenia J Neurosci 23 2003 7407 7411
54. F. Ferrarelli, S. Sarasso, Y. Guller, B.A. Riedner, M.J. Peterson, and M. Bellesi Reduced natural oscillatory frequency of frontal thalamocortical circuits in schizophrenia Arch Gen Psychiatry 69 2012 766 774
55. G. Leicht, S. Karch, E. Karamatskos, I. Giegling, H.J. Möller, and U. Hegerl Alterations of the early auditory evoked gamma-band response in first-degree relatives of patients with schizophrenia: Hints to a new intermediate phenotype J Psychiatr Res 45 2011 699 705
56. J.M. Ford, M. Gray, W.O. Faustman, T.H. Heinks, and D.H. Mathalon Reduced gamma-band coherence to distorted feedback during speech when what you say is not what you hear Int J Psychophysiol 57 2005 143 150
57. C.M. Gray, P. König, A.K. Engel, and W. Singer Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties Nature 338 1989 334 337
58. P.J. Uhlhaas, and S.M. Silverstein Perceptual organization in schizophrenia spectrum disorders: Empirical research and theoretical implications Psychol Bull 131 2005 618 632
59. T. Hashimoto, H.H. Bazmi, K. Mirnics, Q. Wu, A.R. Sampson, and D.A. Lewis Conserved regional patterns of GABA-related transcript expression in the neocortex of subjects with schizophrenia Am J Psychiatry 165 2008 479 489
60. Z.J. Zhang, and G.P. Reynolds A selective decrease in the relative density of parvalbumin-immunoreactive neurons in the hippocampus in schizophrenia Schizophr Res 55 2002 1 10
61. D.J. Lodge, M.M. Behrens, and A.A. Grace A loss of parvalbumin-containing interneurons is associated with diminished oscillatory activity in an animal model of schizophrenia J Neurosci 29 2009 2344 2354
62. T. Sigurdsson, K.L. Stark, M. Karayiorgou, J.A. Gogos, and J.A. Gordon Impaired hippocampal-prefrontal synchrony in a genetic mouse model of schizophrenia Nature 464 2010 763 767
63. L. Sun, N. Castellanos, C. Grützner, D. Koethe, D. Rivolta, and M. Wibral Evidence for dysregulated high-frequency oscillations during sensory processing in medication-naive, first episode schizophrenia Schizophr Res 150 2013 519 525
64. C. Grutzner, M. Wibral, L. Sun, D. Rivolta, W. Singer, K. Maurer, and P.J. Uhlhaas Deficits in high- (>60 Hz) gamma-band oscillations during visual processing in schizophrenia Front Hum Neurosci 7 2013 88
65. J.P. Hamm, C.S. Gilmore, N.A. Picchetti, S.R. Sponheim, and B.A. Clementz Abnormalities of neuronal oscillations and temporal integration to low- and high-frequency auditory stimulation in schizophrenia Biol Psychiatry 69 2011 989 996
66. R.T. Canolty, E. Edwards, S.S. Dalal, M. Soltani, S.S. Nagarajan, and H.E. Kirsch High gamma power is phase-locked to theta oscillations in human neocortex Science 313 2006 1626 1628
67. O. Jensen, M. Bonnefond, and R. VanRullen An oscillatory mechanism for prioritizing salient unattended stimuli Trends Cogn Sci 16 2012 200 206
68. T. Klausberger, L.F. Marton, J. O'Neill, J.H. Huck, Y. Dalezios, and P. Fuentealba Complementary roles of cholecystokinin- and parvalbumin-expressing GABAergic neurons in hippocampal network oscillations J Neurosci 25 2005 9782 9793
69. G. Buzsaki Rhythms of the Brain 2006 Oxford University Press New York
70. D. Pinault N-methyl d-aspartate receptor antagonists ketamine and MK-801 induce wake-related aberrant gamma oscillations in the rat neocortex Biol Psychiatry 63 2008 730 735
71. L.E. Hong, A. Summerfelt, R.W. Buchanan, P. O'Donnell, G.K. Thaker, M.A. Weiler, and A.C. Lahti Gamma and delta neural oscillations and association with clinical symptoms under subanesthetic ketamine Neuropsychopharmacology 35 2010 632 640
72. J.A. Saunders, M.J. Gandal, and S.J. Siegel NMDA antagonists recreate signal-to-noise ratio and timing perturbations present in schizophrenia Neurobiol Dis 46 2012 93 100
73. K.M. Spencer Baseline gamma power during auditory steady-state stimulation in schizophrenia Front Hum Neurosci 5 2012 190
74. M. Kikuchi, T. Hashimoto, T. Nagasawa, T. Hirosawa, Y. Minabe, and M. Yoshimura Frontal areas contribute to reduced global coordination of resting-state gamma activities in drug-naive patients with schizophrenia Schizophr Res 130 2011 187 194
75. L. Rutter, F.W. Carver, T. Holroyd, S.R. Nadar, J. Mitchell-Francis, and J. Apud Magnetoencephalographic gamma power reduction in patients with schizophrenia during resting condition Hum Brain Mapp 30 2009 3254 3264
76. P.J. Uhlhaas, G. Pipa, S. Neuenschwander, M. Wibral, and W. Singer A new look at gamma? High- (>60 Hz) gamma-band activity in cortical networks: function, mechanisms and impairment Prog Biophys Mol Biol 105 2011 14 28
77. C. Basar-Eroglu, C. Schmiedt-Fehr, B. Mathes, J. Zimmermann, and A. Brand Are oscillatory brain responses generally reduced in schizophrenia during long sustained attentional processing? Int J Psychophysiol 71 2009 75 83
78. C. Schmiedt, A. Brand, H. Hildebrandt, and C. Basar-Eroglu Event-related theta oscillations during working memory tasks in patients with schizophrenia and healthy controls Brain Res Cogn Brain Res 25 2005 936 947
79. T.G. Popov, B.S. Rockstroh, P. Popova, A.M. Carolus, and G.A. Miller Dynamics of alpha oscillations elucidate facial affect recognition in schizophrenia Cogn Affect Behav Neurosci 14 2014 364 377
80. F. Roux, M. Wibral, W. Singer, J. Aru, and P.J. Uhlhaas The phase of thalamic alpha activity modulates cortical gamma-band activity: Evidence from resting-state MEG recordings J Neurosci 33 2013 17827 17835
81. D. Osipova, D. Hermes, and O. Jensen Gamma power is phase-locked to posterior alpha activity PLoS One 3 2008 e3990
82. O. Jensen, and L.L. Colgin Cross-frequency coupling between neuronal oscillations Trends Cogn Sci 11 2007 267 269
83. K. Kirihara, A.J. Rissling, N.R. Swerdlow, D.L. Braff, and G.A. Light Hierarchical organization of gamma and theta oscillatory dynamics in schizophrenia Biol Psychiatry 71 2012 873 880
84. J. Aru, J. Aru, V. Priesemann, M. Wibral, L. Lana, and G. Pipa Untangling cross-frequency coupling in neuroscience Curr Opin Neurobiol 31C 2014 51 61
85. E. Bleuler Dementia Praecox or the Group of Schizophrenias 1911 International Universities Press New York
86. P.E. Meehl Schizotaxia revisited Arch Gen Psychiatry 46 1989 935 944
87. L. Sullwold, and G. Huber Basic schizophrenic disorders Monogr Gesamtgeb Psychiatr Psychiatry Ser 42 1986 1 177
88. F. Schultze-Lutter Subjective symptoms of schizophrenia in research and the clinic: The basic symptom concept Schizophr Bull 35 2009 5 8
89. J. Parnas A disappearing heritage: The clinical core of schizophrenia Schizophr Bull 37 2011 1121 1130
90. S. Kapur Psychosis as a state of aberrant salience: A framework linking biology, phenomenology, and pharmacology in schizophrenia Am J Psychiatry 160 2003 13 23
91. T.A. Ward, K.J. Gaynor, M.D. Hunter, P.W. Woodruff, P.A. Garety, and E.R. Peters Appraisals and responses to experimental symptom analogues in clinical and nonclinical individuals with psychotic experiences Schizophr Bull 40 2014 845 855
92. R.C. Gur, M.E. Calkins, T.D. Satterthwaite, K. Ruparel, W.B. Bilker, and T.M. Moore Neurocognitive growth charting in psychosis spectrum youths JAMA Psychiatry 71 2014 366 374
93. F. Schultze-Lutter, S. Ruhrmann, P. Fusar-Poli, A. Bechdolf, B.G. Schimmelmann, and J. Klosterkötter Basic symptoms and the prediction of first-episode psychosis Curr Pharm Des 18 2012 351 357
94. P. Fusar-Poli, S. Borgwardt, A. Bechdolf, J. Addington, A. Riecher-Rössler, and F. Schultze-Lutter The psychosis high-risk state: A comprehensive state-of-the-art review JAMA Psychiatry 70 2013 107 120
95. P.J. Uhlhaas, F. Roux, W. Singer, C. Haenschel, R. Sireteanu, and E. Rodriguez The development of neural synchrony reflects late maturation and restructuring of functional networks in humans Proc Natl Acad Sci U S A 106 2009 9866 9871
96. T. Hashimoto, Q.L. Nguyen, D. Rotaru, T. Keenan, D. Arion, and M. Beneyto Protracted developmental trajectories of GABAA receptor alpha1 and alpha2 subunit expression in primate prefrontal cortex Biol Psychiatry 65 2009 1015 1023
97. H.X. Wang, and W.J. Gao Cell type-specific development of NMDA receptors in the interneurons of rat prefrontal cortex Neuropsychopharmacology 34 2009 2028 2040
98. K.Y. Tseng, and P. O'Donnell Dopamine modulation of prefrontal cortical interneurons changes during adolescence Cereb Cortex 17 2007 1235 1240
99. P.J. Uhlhaas, and W. Singer The development of neural synchrony and large-scale cortical networks during adolescence: Relevance for the pathophysiology of schizophrenia and neurodevelopmental hypothesis Schizophr Bull 37 2011 514 523
100. J.R. Hollerman, and W. Schultz Dopamine neurons report an error in the temporal prediction of reward during learning Nat Neurosci 1 1998 304 309
101. D.R. Rosenberg, and D.A. Lewis Postnatal maturation of the dopaminergic innervation of monkey prefrontal and motor cortices: A tyrosine hydroxylase immunohistochemical analysis J Comp Neurol 358 1995 383 400
102. P.S. Goldman-Rakic, and R.M. Brown Postnatal development of monoamine content and synthesis in the cerebral cortex of rhesus monkeys Brain Res 256 1982 339 349
103. B.C. Ho, N.C. Andreasen, S. Ziebell, R. Pierson, and V. Magnotta Long-term antipsychotic treatment and brain volumes: A longitudinal study of first-episode schizophrenia Arch Gen Psychiatry 68 2011 128 137
104. H. Tost, D.F. Braus, S. Hakimi, M. Ruf, C. Vollmert, F. Hohn, and A. Meyer-Lindenberg Acute D2 receptor blockade induces rapid, reversible remodeling in human cortical-striatal circuits Nat Neurosci 13 2010 920 922
105. T. Womelsdorf, T.A. Valiante, N.T. Sahin, K.J. Miller, and P. Tiesinga Dynamic circuit motifs underlying rhythmic gain control, gating and integration Nat Neurosci 17 2014 1031 1039
106. N. Koutsouleris, C. Davatzikos, R. Bottlender, K. Patschurek-Kliche, J. Scheuerecker, and P. Decker Early recognition and disease prediction in the at-risk mental states for psychosis using neurocognitive pattern classification Schizophr Bull 38 2012 1200 1215
107. R.W. Buchanan, R.S. Keefe, J.A. Lieberman, D.M. Barch, J.G. Csernansky, and D.C. Goff A randomized clinical trial of MK-0777 for the treatment of cognitive impairments in people with schizophrenia Biol Psychiatry 69 2011 442 449
108. D. Umbricht, D. Alberati, M. Martin-Facklam, E. Borroni, E.A. Youssef, and M. Ostland Effect of bitopertin, a glycine reuptake inhibitor, on negative symptoms of schizophrenia: A randomized, double-blind, proof-of-concept study JAMA Psychiatry 71 2014 637 646
109. K.M. Gill, J.M. Cook, M.M. Poe, and A.A. Grace Prior antipsychotic drug treatment prevents response to novel antipsychotic agent in the methylazoxymethanol acetate model of schizophrenia Schizophr Bull 40 2014 341 350
110. Y. Du, and A.A. Grace Peripubertal diazepam administration prevents the emergence of dopamine system hyperresponsivity in the MAM developmental disruption model of schizophrenia Neuropsychopharmacology 38 2013 1881 1888
111. J.H. Cabungcal, D.S. Counotte, E.M. Lewis, H.A. Tejeda, P. Piantadosi, and C. Pollock Juvenile antioxidant treatment prevents adult deficits in a developmental model of schizophrenia Neuron 83 2014 1073 1084
112. H. Lee, D. Dvorak, H.Y. Kao, Á.M. Duffy, H.E. Scharfman, and A.A. Fenton Early cognitive experience prevents adult deficits in a neurodevelopmental schizophrenia model Neuron 75 2012 714 724
113. M. van der Gaag, D.H. Nieman, J. Rietdijk, S. Dragt, H.K. Ising, and R.M. Klaassen Cognitive behavioral therapy for subjects at ultrahigh risk for developing psychosis: A randomized controlled clinical trial Schizophr Bull 38 2012 1180 1188